Bupropion for the treatment of apathy in Huntington's disease: A multicenter, randomised, double-blind, placebocontrolled, prospective crossover trial

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Gelderblom, Harald ^a,h   Wüstenberg, Torsten ^a   McLean, Tim ^b   Mütze, Lisanne ^b   Fischer, Wilhelm ^c   Saft, Carsten ^d   Hoffmann, Rainer ^d   Süssmuth, Sigurd ^b   Schlattmann, Peter ^e   Van Duijn, Erik ^f   Landwehrmeyer, Bernhard ^b,c   Priller, Josef ^a,g  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b European Huntington's Disease Network (EHDN)   (Germany)

^c UNIVERSITY OF ULM   (Germany)

^d ST JOSEF HOSPITAL   (Germany)

^e Institute of Medical Statistics Computer Science and Documentation   (Germany)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^g GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^h National Association of Statutory Health Insurance Funds   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMFEBUTAMONE; DOPAMINE RECEPTOR; PLACEBO; ANTIDEPRESSANT AGENT;

ADULT; AGED; APATHY; APATHY EVALUATION SCALE; ARTICLE; BASAL GANGLION; CAREGIVER; CLINICAL ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DISEASE COURSE; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; DRUG SAFETY; FEMALE; FUNCTIONAL CONNECTIVITY; GAMBLING; HUMAN; HUNTINGTON CHOREA; MALE; MENTAL DISEASE; MINI MENTAL STATE EXAMINATION; MULTICENTER STUDY; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME VARIABLE; PATHOPHYSIOLOGY; PHASE 2 CLINICAL TRIAL; PREFRONTAL CORTEX; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; RATING SCALE; SCORING SYSTEM; STROOP TEST; STRUCTURED INTERVIEW; SYMPTOMATOLOGY; UNIFIED HUNTINGTON DISEASE RATING SCALE; VENTROLATERAL PREFRONTAL CORTEX; BRAIN; CLINICAL TRIAL; DIAGNOSTIC IMAGING; DRUG EFFECTS; FUNCTIONAL NEUROIMAGING; HUNTINGTON DISEASE; MIDDLE AGED; PSYCHOLOGY; REWARD; TREATMENT OUTCOME;

ADULT; AGED; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; APATHY; BRAIN; BUPROPION; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; HUNTINGTON DISEASE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; REWARD; TREATMENT OUTCOME;

EID: 85016040835     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0173872     Document Type: Article

References (49)

1. Craufurd D, Thompson JC, Snowden JS. Behavioral changes in Huntington Disease. Neuropsychiatry, neuropsychology, and behavioral neurology. 2001; 14(4):219-26. PMID: 11725215
2. Levy R, Dubois B. Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cerebral cortex. 2006; 16(7):916-28. https://doi.org/10.1093/cercor/bhj043 PMID: 16207933
3. Starkstein SE, Leentjens AF. The nosological position of apathy in clinical practice. Journal of neurology, neurosurgery, and psychiatry. 2008; 79(10):1088-92. https://doi.org/10.1136/jnnp.2007.136895 PMID: 18187477
4. Tabrizi SJ, Scahill RI, Owen G, Durr A, Leavitt BR, Roos RA, et al. Predictors of phenotypic progression and disease onset in premanifest and early-stage Huntington's disease in the TRACK-HD study: analysis of 36-month observational data. The Lancet Neurology. 2013; 12(7):637-49. https://doi.org/10.1016/S1474-4422(13)70088-7 PMID: 23664844
5. van Duijn E, Craufurd D, Hubers AA, Giltay EJ, Bonelli R, Rickards H, et al. Neuropsychiatric symptoms in a European Huntington's disease cohort (REGISTRY). Journal of neurology, neurosurgery, and psychiatry. 2014; 85(12):1411-8. https://doi.org/10.1136/jnnp-2013-307343 PMID: 24828898
6. Baudic S, Maison P, Dolbeau G, Boisse MF, Bartolomeo P, Dalla Barba G, et al. Cognitive impairment related to apathy in early Huntington's disease. Dementia and geriatric cognitive disorders. 2006; 21(5-6):316-21. https://doi.org/10.1159/000091523 PMID: 16484810
7. Schwab LC, Garas SN, Drouin-Ouellet J, Mason SL, Stott SR, Barker RA. Dopamine and Huntington's disease. Expert review of neurotherapeutics. 2015:1-14.
8. Andre VM, Cepeda C, Levine MS. Dopamine and glutamate in Huntington's disease: A balancing act. CNS neuroscience & therapeutics. 2010; 16(3):163-78.
9. Roze E, Cahill E, Martin E, Bonnet C, Vanhoutte P, Betuing S, et al. Huntington's Disease and Striatal Signaling. Frontiers in neuroanatomy. 2011; 5:55. https://doi.org/10.3389/fnana.2011.00055 PMID: 22007160
10. Dogan I, Eickhoff SB, Schulz JB, Shah NJ, Laird AR, Fox PT, et al. Consistent neurodegeneration and its association with clinical progression in Huntington's disease: a coordinate-based meta-analysis. Neuro-degenerative diseases. 2013; 12(1):23-35. https://doi.org/10.1159/000339528 PMID: 22922585
11. Thompson JC, Harris J, Sollom AC, Stopford CL, Howard E, Snowden JS, et al. Longitudinal evaluation of neuropsychiatric symptoms in Huntington's disease. The Journal of neuropsychiatry and clinical neurosciences. 2012; 24(1):53-60. https://doi.org/10.1176/appi.neuropsych.11030057 PMID: 22450614
12. Douaud G, Gaura V, Ribeiro MJ, Lethimonnier F, Maroy R, Verny C, et al. Distribution of grey matter atrophy in Huntington's disease patients: a combined ROI-based and voxel-based morphometric study. NeuroImage. 2006; 32(4):1562-75. https://doi.org/10.1016/j.neuroimage.2006.05.057 PMID: 16875847
13. Fennema-Notestine C, Archibald SL, Jacobson MW, Corey-Bloom J, Paulsen JS, Peavy GM, et al. In vivo evidence of cerebellar atrophy and cerebral white matter loss in Huntington disease. Neurology. 2004; 63(6):989-95. PMID: 15452288
14. Kassubek J, Juengling FD, Kioschies T, Henkel K, Karitzky J, Kramer B, et al. Topography of cerebral atrophy in early Huntington's disease: a voxel based morphometric MRI study. Journal of neurology, neurosurgery, and psychiatry. 2004; 75(2):213-20. PMID: 14742591
15. Schott BH, Minuzzi L, Krebs RM, Elmenhorst D, Lang M, Winz OH, et al. Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J Neurosci. 2008; 28(52):14311-9. https://doi.org/10.1523/JNEUROSCI. 2058-08.2008 PMID: 19109512
16. Knutson B, Westdorp A, Kaiser E, Hommer D. FMRI visualization of brain activity during a monetary incentive delay task. NeuroImage. 2000; 12(1):20-7. https://doi.org/10.1006/nimg.2000.0593 PMID: 10875899
17. Enzi B, Edel MA, Lissek S, Peters S, Hoffmann R, Nicolas V, et al. Altered ventral striatal activation during reward and punishment processing in premanifest Huntington's disease: a functional magnetic resonance study. Exp Neurol. 2012; 235(1):256-64. https://doi.org/10.1016/j.expneurol.2012.02.003 PMID: 22366326
18. Krishnamoorthy A, Craufurd D. Treatment of Apathy in Huntington's Disease and Other Movement Disorders. Current treatment options in neurology. 2011; 13(5):508-19. https://doi.org/10.1007/s11940-011-0140-y PMID: 21800056
19. Mason SL, Barker RA. Advancing pharmacotherapy for treating Huntington's disease: a review of the existing literature. Expert Opin Pharmacother. 2015:1-12.
20. Marin RS, Fogel BS, Hawkins J, Duffy J, Krupp B. Apathy: a treatable syndrome. The Journal of neuropsychiatry and clinical neurosciences. 1995; 7(1):23-30. https://doi.org/10.1176/jnp.7.1.23 PMID: 7711487
21. Corcoran C, Wong ML, O'Keane V. Bupropion in the management of apathy. J Psychopharmacol. 2004; 18(1):133-5. https://doi.org/10.1177/0269881104043284 PMID: 15107198
22. Strassburger K AJ, Saft C. Bupropion: first experience in Huntington's Disease. J Neurol, Neurosurg Psychiatry 2008; 79:A29-30.
23. Paul RH, Brickman AM, Navia B, Hinkin C, Malloy PF, Jefferson AL, et al. Apathy is associated with volume of the nucleus accumbens in patients infected with HIV. The Journal of neuropsychiatry and clinical neurosciences. 2005; 17(2):167-71. https://doi.org/10.1176/appi.neuropsych.17.2.167 PMID: 15939969
24. Lorenz RC, Gleich T, Beck A, Pohland L, Raufelder D, Sommer W, et al. Reward anticipation in the adolescent and aging brain. Hum Brain Mapp. 2014; 35(10):5153-65. https://doi.org/10.1002/hbm.22540 PMID: 24801222
25. Starkstein SE, Ingram L, Garau ML, Mizrahi R. On the overlap between apathy and depression in dementia. Journal of neurology, neurosurgery, and psychiatry. 2005; 76(8):1070-4. https://doi.org/10.1136/jnnp.2004.052795 PMID: 16024880
26. Marin RS. Apathy: a neuropsychiatric syndrome. The Journal of neuropsychiatry and clinical neurosciences. 1991; 3(3):243-54. https://doi.org/10.1176/jnp.3.3.243 PMID: 1821241
27. Marin RS, Biedrzycki RC, Firinciogullari S. Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res. 1991; 38(2):143-62. PMID: 1754629
28. Unified Huntington's Disease Rating Scale: reliability and consistency. Huntington Study Group. Movement disorders: official journal of the Movement Disorder Society. 1996; 11(2):136-42.
29. McCarrey AC, Henry JD, von Hippel W, Weidemann G, Sachdev PS, Wohl MJ, et al. Age differences in neural activity during slot machine gambling: an fMRI study. PLoS One. 2012; 7(11):e49787. https://doi.org/10.1371/journal.pone.0049787 PMID: 23209599
30. Weiser M, Garibaldi G. Quantifying motivational deficits and apathy: a review of the literature. Eur Neuropsychopharmacol. 2015; 25(8):1060-81. https://doi.org/10.1016/j.euroneuro.2014.08.018 PMID: 25863434
31. Robert P, Onyike CU, Leentjens AF, Dujardin K, Aalten P, Starkstein S, et al. Proposed diagnostic criteria for apathy in Alzheimer's disease and other neuropsychiatric disorders. European psychiatry: the journal of the Association of European Psychiatrists. 2009; 24(2):98-104.
32. Mason S, Barker RA. Rating Apathy in Huntington's Disease: Patients and Companions Agree. Journal of Huntington's disease. 2015; 4(1):49-59. PMID: 26333257
33. Duff K, Paulsen JS, Beglinger LJ, Langbehn DR, Wang C, Stout JC, et al. "Frontal" behaviors before the diagnosis of Huntington's disease and their relationship to markers of disease progression: evidence of early lack of awareness. The Journal of neuropsychiatry and clinical neurosciences. 2010; 22 (2):196-207. https://doi.org/10.1176/appi.neuropsych.22.2.196 PMID: 20463114
34. Lueken U, Seidl U, Schwarz M, Volker L, Naumann D, Mattes K, et al. [Psychometric properties of a German version of the Apathy Evaluation Scale]. Fortschritte der Neurologie-Psychiatrie. 2006; 74 (12):714-22. https://doi.org/10.1055/s-2006-932164 PMID: 17167730
35. Clarke DE, Ko JY, Kuhl EA, van Reekum R, Salvador R, Marin RS. Are the available apathy measures reliable and valid? A review of the psychometric evidence. Journal of psychosomatic research. 2011; 70 (1):73-97. https://doi.org/10.1016/j.jpsychores.2010.01.012 PMID: 21193104
36. Hsieh CJ, Chu H, Cheng JJ, Shen WW, Lin CC. Validation of apathy evaluation scale and assessment of severity of apathy in Alzheimer's disease. Psychiatry Clin Neurosci. 2012; 66(3):227-34. https://doi.org/10.1111/j.1440-1819.2011.02315.x PMID: 22443245
37. Mulin E, Leone E, Dujardin K, Delliaux M, Leentjens A, Nobili F, et al. Diagnostic criteria for apathy in clinical practice. International journal of geriatric psychiatry. 2011; 26(2):158-65. https://doi.org/10.1002/gps.2508 PMID: 20690145
38. Lane-Brown AT, Tate RL. Measuring apathy after traumatic brain injury: Psychometric properties of the Apathy Evaluation Scale and the Frontal Systems Behavior Scale. Brain injury. 2009; 23(13-14):999-1007. https://doi.org/10.3109/02699050903379347 PMID: 19891539
39. Cummings J, Friedman JH, Garibaldi G, Jones M, Macfadden W, Marsh L, et al. Apathy in Neurodegenerative Diseases: Recommendations on the Design of Clinical Trials. Journal of geriatric psychiatry and neurology. 2015; 28(3):159-73. https://doi.org/10.1177/0891988715573534 PMID: 25809634
40. Chatterjee A, Anderson KE, Moskowitz CB, Hauser WA, Marder KS. A comparison of self-report and caregiver assessment of depression, apathy, and irritability in Huntington's disease. The Journal of neuropsychiatry and clinical neurosciences. 2005; 17(3):378-83. https://doi.org/10.1176/jnp.17.3.378 PMID: 16179661
41. Mestre TA, van Duijn E, Davis AM, Bachoud-Levi AC, Busse M, Anderson KE, et al. Rating scales for behavioral symptoms in Huntington's disease: Critique and recommendations. Movement disorders: official journal of the Movement Disorder Society. 2016; 31(10):1466-78.
42. Ho AK, Robbins AO, Barker RA. Huntington's disease patients have selective problems with insight. Movement disorders: official journal of the Movement Disorder Society. 2006; 21(3):385-9.
43. Hoth KF, Paulsen JS, Moser DJ, Tranel D, Clark LA, Bechara A. Patients with Huntington's disease have impaired awareness of cognitive, emotional, and functional abilities. Journal of clinical and experimental neuropsychology. 2007; 29(4):365-76. https://doi.org/10.1080/13803390600718958 PMID: 17497560
44. Starkstein SE. Anosognosia in Alzheimer's disease: diagnosis, frequency, mechanism and clinical correlates. Cortex; a journal devoted to the study of the nervous system and behavior. 2014; 61:64-73. https://doi.org/10.1016/j.cortex.2014.07.019 PMID: 25481465
45. Pfeifer L, Drobetz R, Fankhauser S, Mortby ME, Maercker A, Forstmeier S. Caregiver rating bias in mild cognitive impairment and mild Alzheimer's disease: impact of caregiver burden and depression on dyadic rating discrepancy across domains. International psychogeriatrics/IPA. 2013; 25(8):1345-55.
46. Bonnelle V, Veromann KR, Burnett Heyes S, Lo Sterzo E, Manohar S, Husain M. Characterization of reward and effort mechanisms in apathy. Journal of physiology, Paris. 2014.
47. de Yebenes JG, Landwehrmeyer B, Squitieri F, Reilmann R, Rosser A, Barker RA, et al. Pridopidine for the treatment of motor function in patients with Huntington's disease (MermaiHD): a phase 3, randomised, double-blind, placebo-controlled trial. The Lancet Neurology. 2011; 10(12):1049-57. https://doi.org/10.1016/S1474-4422(11)70233-2 PMID: 22071279
48. Huntington Study G, Frank S, Testa CM, Stamler D, Kayson E, Davis C, et al. Effect of Deutetrabenazine on Chorea Among Patients With Huntington Disease: A Randomized Clinical Trial. JAMA. 2016; 316(1):40-50. https://doi.org/10.1001/jama.2016.8655 PMID: 27380342
49. Cubo E, Gonzalez M, del Puerto I, de Yebenes JG, Arconada OF, Gabriel y Galan JM, et al. Placebo effect characteristics observed in a single, international, longitudinal study in Huntington's disease. Movement disorders: official journal of the Movement Disorder Society. 2012; 27(3):439-42.